REVIEW

Essential oil production: relationship with abundance of glandulartrichomes in aerial surface of plants

Kamal K. Biswas Æ Adam J. Foster ÆTheingi Aung Æ Soheil S. Mahmoud

Received: 26 October 2007 / Revised: 20 May 2008 / Accepted: 25 August 2008 / Published online: 16 September 2008

� Franciszek Gorski Institute of Plant Physiology, Polish Academy of Sciences, Krakow 2008

Abstract The terpenoids, or isoprenoids, are a large family

of natural products that are best known as constituents of

the essential oils in plants. Because of their pleasant flavor

and aromatic properties, essential oils have an economic

importance in perfumery, cosmetic, pharmaceutical and

various other industries. However, expression profiles of

regulatory genes in essential oil production have not been

dissected entirely, which may be an interesting topic of

future research. In this report, we review recent studies on

isoprenoids biosynthesis in plants. We also discuss the pro-

gress of our recent research activities on isoprenoid studies.

Keywords Isoprenoid � Glandular trichome � Lavender

Introduction

The glandular trichome provides an excellent system to

study isoprenoid biosynthesis in plants. Techniques were

developed to isolate and purify the glandular cells in dif-

ferent plant species. For instance, glandular trichomes from

Artemisia annua were used for cDNA library construction

to understand the biosynthesis of artemisinin, an antima-

larial sesquiterpene (Teoh et al. 2006). Plants have evolved

in various ways to protect themselves or attract insects for

pollination. For example, conifers secrete a complex mix-

ture of monoterpenes, sesquiterpenes and diterpenes,

termed oleoresin, in response to attack by insect predators

(Keeling and Bohlmann 2006; Helmig et al. 2007) and

glandular trichomes in Geranium spp. have been shown to

secrete a viscous exudate that provides a defense mecha-

nism against athropods (Gerholo et al. 1984; Walters et al.

1989; Hesk et al. 1990; Hare and Elle 2002). Osmophores,

a form of glandular epidermis common in floral tissues,

secrete volatile compounds responsible for attracting poll-

inators (Lehnebach and Robertson 2004). Thus, glandular

trichome is very important for aromatic plant species to

produce and store essential oils.

Mechanisms of the regulatory genes that control essen-

tial oil production in plants are an area of interest that

needs to be elucidated in greater detail. Transcription fac-

tors have been predicted to be the regulatory proteins that

modulate the expression of genes or gene groups in dif-

ferent plants. For example, expression of the ISPS

(isoprenoid synthase) gene in poplar is regulated by the

transcriptional factors LHY (late hypocotyl) and CCA1

(circadian clock associated 1) (Loivamaki et al. 2007).

Similarly, ttg1 (transparent testa glabrous), a transcription

factor influences flavonoid biosynthesis in Arabidopsis

(Galway et al. 1994). However, transcription factors reg-

ulating monoterpene biosynthesis in plants have yet to be

reported. We cloned putative sequences of the linallol

synthase (LIS) gene promoter from leaves and flowers of

Lavandula angustifolia (Lady Lavender). These sequences

contain the TATA box and transcription factor binding

sites (data not shown). We are in process of developing

transgenic plants with LIS-promoter that may become

important tools for functional analyses of the linalool

synthesis genes in Lavenders (Lavandula species).

Communicated by A. Kononowicz.

K. K. Biswas (&) � A. J. Foster � T. Aung

Department of Biological Sciences, Simon Fraser University,

8888 University Drive, Burnaby, BC V5A 1S6, Canada

e-mail: kamal_biswas@sfu.ca

S. S. Mahmoud

Chemistry and Earth and Environmental Sciences,

University of British Columbia Okanagan,

3333 University Way, Kelowna, BC V1V 1V7, Canada

123

Acta Physiol Plant (2009) 31:13–19

DOI 10.1007/s11738-008-0214-y

Pathways in isoprenoid biosynthesis in plants

Isoprenoids are derived from the condensation of the 5-

carbon unit isopentyl diphosphate (IPP) and its isomer

dimethylallyl diphosphate (DMAPP) in a head-to-tail or

head-to-head fashion. Depending on the number of iso-

prene units linked together, terpenes are classified into

hemiterpenes (C5), monoterpenes (C10), sesquiterpenes

(C15), diterpenes (C20), sesterpenes (C25), triterpenes

(C30), and tetraterpenes (C40).

In higher plants, two independent pathways, the meva-

lonate (MVA) and the methylerythritol (MEP), are

believed to be responsible for the formation of IPP (iso-

pentyl diphosphate) and DMAPP (Enfissi et al. 2005;

Bartram et al. 2006; Kobayashi et al. 2007).

Historically, it was believed that IPP and DMAPP were

solemnly synthesized via MVA, in the cytosol. This pro-

cess involves three key steps (Lichtenthaler 1999; Liu et al.

2005). First, three molecules of acetyl-CoA couple to yield

3-hydroxy-3-methylglutaryl CoA, which is subsequently

reduced by the enzyme HMG CoA reductase to yield

mevalonic acid. In the next two steps, mevalonate kinase

and mevalonate-5-phosphate kinase phosphorylate MVA to

form mevalonate-5-diphosphate, which is subsequently

decarboxylated to yield IPP. In mammals and fungi, flux

through this pathway is highly regulated by the activity of

HMGR (Chappell et al. 1995). However, studies investi-

gating the regulatory role of HMGR in terpene synthesis

yielded contradictory results in plants. For example, over-

expression of Hamster HMGR in tobacco plants favored

the accumulation of total sterols, while levels of other

isoprenoids such as carotenoids or the phytol chain of

chlorophyll remained relatively unaltered in the transgenic

plants (Chappell et al. 1995). This antagonism could be

explained by the discovery of a mevalonate independent

plastidal pathway for IPP synthesis, termed 1-deoxyxylu-

lose-5-phosphate (DXP) or 2-C-methyl-D-erythritol-4-

phosphate (MEP) (Lange et al. 1998; Takahashi et al. 1998;

Eisenreich et al. 2001; Bertomeu et al. 2006; Kobayashi

et al. 2007).

The plastidal pathways start with the transketolase-type

condensation of pyruvate and glyceraldehyde-3-phosphate

to form DXP, followed by the rearrangement and reduction

of DXP to MEP, formation of the cytidine-50-diphosphate

derivative (CDP-ME), phosphorylation at C2 (CDP-MEP),

cyclization to 2-C-methylerythritol-2,4-cyclodiphosphate

(cMEPP), and the reductive ring opening to 1-hydroxy-2

methyl-2-(E)-butenyl 4-diphosphate (HMBPP). Isopentyl

diphosphate (IPP) and DMAPP are produced as final prod-

ucts (Lichtenthaler 1999; Herz et al. 2000; Concepcion and

Boronat 2002; Rohdich et al. 2002; Enfissi et al. 2005). IPP

and DMAPP are condensed to yield geranyl diphosphate

(GPP), farnesyl pyrophosphate (FPP) and geranylgeranyl

pyrophosphate (GGFP), which are the building blocks for all

monoterpene, sesqui- and diterpenes, respectively (Fig. 1).

Isolation of mutants that are defective or impaired for

specific response is an important step to understand in

detail the regulatory mechanism. A report showed that the

strict separation of the MVA and MVA-independent

pathways might not exist, practically. This result was

explained through the blocking of both MVA and MEP

with inhibitors (Bartram et al. 2006). In a recent study,

Kobayashi et al. (2007), demonstrated that the loi1 (lova-

statin insentive 1) mutant of Arabidopsis is resistant to

lovastatin and clomazone, inhibitors of the MVA and MEP,

respectively. Isoprenoid biosynthetic pathways have been

characterized in other plant species (Concepcion 2004;

Enfissi et al. 2005). Considering the recent progress, an

attempt was undertaken to construct two cDNA libraries

with Lavender flowers and with leaves. Approximately,

15,000 ESTs have been sequenced, where 495 clones are

closely related to important steps of isoprenoid biosyn-

thesis. Among them, 15 clones related to MVA or MEP

were analyzed in three different Lavender varieties for the

tissue-specific expression with real time PCR. We expect

promising results regarding tissue-specific expression soon.

Glandular trichomes: source for essential oil

production in plants

Plants produce both non-glandular and glandular trichomes

that play different roles. Non-glandular trichomes are

typically simple hairs usually found on the aerial surfaces

of plants including Arabidopsis (Marks 1997; Hase et al.

2006). Glandular trichomes are one of the most common

secretory structures that produce and store essential oils in

plants (Iijima et al. 2004; Covello et al. 2007). Despite their

importance, detailed physiological roles as well as the

genetic backgrounds of glandular trichome development

remain obscure, possibly due to the low abundance of

secretory cells within glandular trichomes. Some studies do

suggest physiological roles for glandular trichomes, but

lack supporting data. However, in Phillyrea latifolia, light-

induced synthesis of flavenoids in glandular trichomes was

shown to inactivate polypropenoid metabolism allowing

for acclimatization (Tattini et al. 2000).

Development and distribution of glandular trichomes in

peppermint was discussed in previous works by Turner

et al. (2000a, b). Two broad morphological types of glan-

dular trichomes: capitate and peltate have been defined in

plants. Abundance of glandular trichomes in plants and

their relationship with essential oil production in many

plants including peppermint (McCaskill and Croteau 1995;

McCaskill and Croteau 1999; McConkey et al. 2000; Lange

et al. 2000; Turner et al. 2000a, b; Mahmoud and Croteau

14 Acta Physiol Plant (2009) 31:13–19

123

2003; Mahmoud et al. 2004; Ringer et al. 2005; Hyatt et al.

2007), lima bean (Bartram et al. 2006; Pinto et al. 2007),

Lavender (Behnam et al. 2006; Bertomeu et al. 2006), and

tomato (Li et al. 2004; Enfissi et al. 2005; Fridman et al.

2005), have been discussed, which has enriched our

understanding of isoprenoid biosynthesis in plants.

The morphology and cytology of glandular trichomes in

Lavender is well documented (Werker et al. 1993; Copetta

et al. 2006). Lamiaceae species that produce aromatic oils

possesses both capitate and peltate glandular trichomes.

Both types of glandular trichomes are composed of a single

basal cell, a one-stalk cell and a head. Capitate glandular

trichomes possess a one- or two-celled head, while the head

of peltate cells contains four or more broad cells (Werker

et al. 1993). Secreted materials in peltate glandular tric-

homes vary substantially in compostition and quantity

related to age and location on a leaf (Maffei et al. 1989;

Werker et al. 1993).

Microorganisms can influence the formation and

chemistry of glandular trichomes. Arbuscular mycorrhiza

(AM) influence the number of peltate glandular trichomes

and their essential oil composition in Ocimum basilicum

(Copetta et al. 2006) and Artemisia annua (Kapoor et al.

2007). The purpose and mechanisms behind the modifica-

tion of glandular trichomes by AM fungi is nsot fully

understood.

Boughton et al. (2005) documented the role of hor-

mone-signaling components in the development of

glandular trichomes in tomato. In another study, Li et al.

(2004) demonstrated that the jai1 mutant of tomato pro-

duces a lower number of glandular trichomes in fruit,

compared to the fruits produced in wild-type plants.

Interestingly, monoterpene productions in jai1 fruits were

below detection levels. In contrast, production of mono-

terpene including a- and b-pinene, limonene, and cis

b-ocimine were high in wild-type fruits. This observation

addresses two points: first, the abundance of glandular

trichomes is correlated with monoterpene production;

second, the hormone-signaling component is somehow

connected with monoterpene production via glandular

trichome development.

There are reports on the role of glandular trichomes in

the production of different compounds that are important in

chemical and pharmaceutical industries (Hare and Walling

2006). One example is the isolation of antidiabetic and

antihypertensive agents from the glandular trichomes in

Vaccinium arctostaphylos (Nickavar et al. 2003). Produc-

tion of antibiotics and insecticides from glandular

trichomes in tomato has been reported in other studies

(Selvanarayanan and Muthukumaran 2005). A series of

reports demonstrated that glandular trichomes are the site

of artemisinin biosynthesis in Artemisia annua (Bertea

Fig. 1 Overview of isoprenoid biosynthesis in plants modified from Dubey et al. (2003). a Formation of terpenoid precursors. b Formation of

terpenoids from precursors

Acta Physiol Plant (2009) 31:13–19 15

123

et al. 2006; Teoh et al. 2006; Covello et al. 2007). Other

published reports on variation and distribution of glandular

trichomes by environmental stimuli, such as temperature

(Gianfagna et al. 1992) and other abiotic factors (Estrada

et al. 2000; Casteel et al. 2006), show various roles of

glandular trichomes in controlling plant growth and

development.

Promoter cloning: a strategy to identify regulatory

elements

Promoter cloning has been considered one of the most

powerful strategies for identifying the transcription factors

in plants. For instance, cis-regulatory elements, such as

Myb transcription factors were identified in Arabidopsis

through cloning of the chs_H1 gene promoter (Matousek

et al. 2005).

Loivamaki et al. (2007) addressed cloning of PcISPS

(Poplar isoprenoid synthase) gene promoter, where the

putative promoter sequence was fused to the reporter genes

coding for the enzyme GUS and E-GFP (enhanced green

fluorescent protein). These constructs were then introduced

into Arabidopsis to monitor functionality of the gene pro-

moter. In doing so, they identified two circadian elements

LHY (late hypocotyl elongated) and CCA1 (circadian

clock associated 1) and they have shown evidence that

AtLHY binds to the PcISPS promoter fragments. The same

type of strategy was employed to monitor promoter activity

of the terpenoid synthesis genes (At3g25820/At3g25830)

in Arabidopsis (Chen et al. 2004). The potential benefit of

promoter cloning was highlighted in two recent works. In

one study, increased carotenoid accumulation was reported

in Escherichia coli by replacing the native promoter of the

chromosomal isoprenoid genes with the strong bacterio-

phage T5 promoter (Yuan et al. 2006). In a second study

(Babili et al. 2006), a synthetic CrtI (carotene desaturase)

gene was generated under the control of the endosperm-

specific glutelin B1 promoter that is important for

increasing the b-carotene content in Golden Rice. Chen

et al. (2003) showed the promoter activity of terpenoid

volatiles in Arabidopsis. These reports indicate that cloning

of the gene promoter is important to identify regulatory

elements, especially for transcription factor binding sites

on promoter sequences. In our study, we show this strategy

is applicable for the identification of the LIS gene (acces-

sion: DQ263741) promoter in Lavenders (Figs. 2, 3). Our

cloned sequences contain transcription factor binding sites

as well as the TATA box (data not shown). Functional

analysis of the linalool synthase gene promoter is in pro-

gress that may give new insight into identifying regulatory

elements, especially for monoterpene biosynthesis in

plants.

Lavender: a model plant for isoprenoid studies

Lavenders are perennial members of the mint family

(Lamiaceae). Lavender species are commonly cultivated

worldwide as ornamental and medicinal plants. Lavenders

are also commercially grown for the production of their

essential oil, which is extensively used as an additive to

food, cosmetic, pharmaceutical and personal care products.

The essential oil of Lavender (Lavandula angustifolia

Mill.) is mainly comprised of monoterpennes (the C10 class

of isoprenoids), and is produced and stored in the glandular

trichomes (or oil glanda), which cover the surface of the

aerial parts of the plant. Monoterpenes commonly found in

Lavender oils include linalool, linalyl acetate, 1,8-cineol,

B-ocimene (usually both cis- and trans-), terpen, and

camphor. The relative abundance of these isoprenoids

defines the quality of the oil and is mainly determined by

plant genotype. Environmental factors (e.g., light intensity,

length of the day and temperature) also affect isoprenoid

biosynthesis and can significantly influence oil composition

in plants. High-grade Lavender oils contain high percent-

ages of linalool and linalyl acetate, while oil quality

decreases with increasing camphor ratios. Ironically, high

yielding Lavender varieties (e.g., Lavandin; Lavandu-

la intermedia) typically produce low-grade oils. Metabolic

engineering in biosynthetic pathways is an important

attempt to overcome this difficulty.

Dra

Exon 1

GSP1GSP2

AP1AP2

Predicted promoter

LIS promoter (772 bp)

(a)

(b)

LIS

Fig. 2 a Schematic representation of Linalool synthase promoter

cloning strategies. Ap1 adaptor primer 1, Ap2 adaptor primer 2, GSP1gene-specific primer1, GSP2 gene-specific primer 2, LIS linalool

synthase promoter, DraI cutting site on top. b Predicted linalool

synthase promoter cloned from young flowers of Lavandulaangustifolia

16 Acta Physiol Plant (2009) 31:13–19

123

An alternative approach is to isolate mutants with

aberrant essential oil production. Agreeing with this view,

we screened a mutant (the EO mutant) from EMS-treated

callus tissues in Lavender. This mutant produced an

essential oil that was drastically different in composition

(the relative abundance of several mono- and sesquiter-

penes) from that of wild type plants. This mutant provides

a useful tool for investigating the regulation of mono- and

sesquiterpene production in plants (data not shown).

Peppermint is often considered as a model species for

isoprenoid studies. Tomato represents another model

system for studying the developmental genetics and

metabolism of glandular trichomes. Some Lavender spe-

cies are grown for essential oil production and are strong

candidates for isoprenoid studies. Earlier studies have

demonstrated the usefulness of Lavender as a species for

genetic transformation (Dronne et al. 1999; Nebauer et al.

2000; Bertomeu et al. 2006). As well, tissue culture prop-

agation of Lavender ex-plants has become very successful.

Combining these traits and genomic resources with the

potential for manipulation of glandular trichomes may

establish Lavender as a model species for isoprenoid

research.

Acknowledgements Grants for this work supported to Soheil

Mahmoud from Natural Sciences and Engineering Research Council

of Canada, Investment Agriculture Foundation of British Columbia,

Western Economic Diversification Canada, Canada Foundation for

Innovation, British Columbia Knowledge Development Fund, and

UBC Okanagan.

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